Deep subsurface microbes

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Introduction

Electron micrograph of the Ebola Zaire virus. This was the first photo ever taken of the virus, on 10/13/1976. By Dr. F.A. Murphy, now at U.C. Davis, then at the CDC.


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Microbes have found a way to exist in every corner of the planet, and humans have found ways to utilize their incredible diversity for thousands of years. From fermenting cheese and wine, to the production of pharmaceuticals, microbes have been utilized for a myriad of reasons. It was not until the late 1920's however, that scientists thought to look deep within the body of our earth itself for a new source of potential biodiversity. Due to the massive amount of habitable area, and the surprising density with which these microbes live, it is now believed that subsurface microbes are responsible for over half of the biomass on the planet [2].

Deep subsurface microbes first came into question when the American geologist Edson S. Bastin questioned why samples of water extracted from oil fields contained hydrogen sulfide and bicarbonates. Armed with the knowledge that certain species of bacteria can derive energy from reducing sulfur compounds in the absence of oxygen, he concluded that there must be populations of these bacteria living in the underground oil reserves, degrading the organic components of oil as a carbon source, and reducing sulfur compounds for energy. By 1926, Bastin and his colleague, Frank E. Greer has cultured sulfur reducing bacteria from samples taken from the groundwater of an oil deposit several hundred meters below the surface. Bastin and Greer's initial deduction was that the bacteria were the ancestors of those buried up to 300 million years ago when the organic materials constituting the oil deposit were buried.

The deeps subsurface ecosystem begins at about 50m below the surface of earths crust, and extends variably downward, up to 2.8km (1.7mi)[1]. The organisms live within the flooded pore space within the rocks and live by reducing inorganic compounds found in the rock. These microbes have some very specific adaptations that allow them to proliferate in such a hostile environment. Radiation resistant, thermophilic, anaerobic microorganisms with a large emphasis on DNA repair mechanisms survive for decades and centuries instead of hours or days. With such a surprising diversity of organisms in such an extreme environment, the deep subsurface has been the subject of many studies in the recent years. They carry out processes that alter the chemical makeup of minerals, degrade pollutants, and alter the mineral content of ground water. Studies are being done to search for deep subsurface microbes that produce antibiotics and heat stable enzymes, and for those that assist in the degradation of toxic substances.

Perhaps the most incredible thing about the microbes found in the deep subsurface, is that the majority of the populations can thrive indefinitely without any input from the earth's surface[1]. That being said, they are effectively 100% disconnected from the rest of life as we know it.

Physical environment

Intense pressures, high temperatures, limited livable space, and limited nutrient availability are all factors that microbes living in this environment must adapt to. It seems that the largest limitation to microbial life in this habitat is temperature, which increases with depth. The highest temperature generally accepted as the livable range for microorganisms in this habitat is 110 degrees C [1] In oceanic crusts, the temperature of the subsurface increases at a rate of about 15 degrees C per kilometer of depth, giving a maximum livable depth of about 7 kilometers. In the continental crusts the rock warms at a significantly faster rate, about 25 degrees C per kilometer, resulting in a maximum livable depth of approximately 4 kilometers [1]. Microbes in these environments can only exist where water fills the pore spaces of rocks. In the marine subsurface, this is rarely an issue, but in continental subsurface, there tends to be a bit more variability in groundwater dispersion.


Hydrothermal Waters

Hydrothermal waters are generally located at tectonically active regions on the ocean floor. Spreading centers and hot spots bring magma relatively close to the surface, which heats the surrounding sediments and rock layers to extremely high temperatures. Hydrothermal subsurface ecosystems are characterized by extreme heat and the presence of sediments comprising both organic and inorganic compounds. The water located in the pore spaces of these deep hydrothermal systems more closely resembles axial hydrothermal vent fluid than typical seawater [2]. Because of this, the microbes inhabiting these ecosystems are almost exclusively thermophilic archea, with a few genera of thermophilic bacteria as well [2].


Sedimentary Basins/Oil Reservoirs

In sedimentary basins and oil reservoirs, it is thought that the microbial communities are remnants from when their ancestors were buried underneath the sediment or organic matter. The nutrients contained within these ecosystems is typically organic matter produced by plants existing at the time when the layers were exposed at the surface. Energy is derived from the reduction of organic compounds in oil or sediments, as well as from inorganic compounds such as sulfur, iron, and manganese [3]. As depth increases, available pore space and nutrient availability decreases, so the metabolic rate of the communities slows down significantly. As the rock becomes increasingly compacted, the colonizable areas become increasingly patchy and isolated, resulting in a plethora of microcommunities surrounding the available sources of nutrients[1].

Crystalline Metamorphic and Igneous Rocks

Igneous rocks are perhaps the most hostile environment in which deep subsurface microbes exist. Due to the processes needed to create igneous rocks, i.e. extreme temperature and pressure, these habitats are effectively sterilized at their creation. Microbes can only colonize the rocks when they have been removed from the hostile surroundings, usually by tectonic processes. Once the rocks cool to below the temperature threshold for microbial life (as far as we know it) the microbes must be transported there by the infiltration of groundwater from above. The groundwater penetrates microscopic fissures and spaces between the crystals and the microbes begin to take hold.

Due to the lack of organic materials in these igneous rocks, the microbial communities are comprised primarily of autotrophs. Their primary source of energy is hydrogen gas, which is produced by reducing iron and sulfur in the presence of oxygen poor water, and gather carbon from carbon dioxide. These microbes, termed "acetogens", excrete organic compounds that can then be utilized by other microbes[1]. These environments are often referred to as "SLiMEs", which stands for subsurface lithoautotrophic microbial ecosystems [1]. These ecosystems can exist indefinitely without any input from the surface.

Microbial communities

Microbial communities are surprisingly diverse in the deep subsurface. Communities consist mainly of bacterial and archeal species that specialize in inorganic substrate reduction, as well as other anaerobes. Microbes exist in a vast range of densities in these ecosystems, from a single cell permanently isolated from all other life, up to 100 million individuals per gram of rock [1]. Densities are a limited by substrate availability and pore space, which sometimes can be so small that only a single cell may fill the void at any given time. The life cycles of these microbes is impressively slow, with cell division occurring up to once per decade, or even once per century [1]. This is in stark contrast to surface microbes, which typically reproduce in a matter of minutes, or months at most.


Key Organisms

Lithotrophs

Thermophiles

Thermophilic metal reducers proliferate throughout the range of deep subsurface microbes [3].

Adaptations

Nutrient Limitations

Most species inhabiting these depths have evolved the ability to reduce inorganic compounds contained within the rocks. These organisms typically use the inorganic compounds, such as iron and sulfur, in conjunction with water to produce the hydrogen gas from which they get their energy. There are some heterotrophic species that exist in these ecosystems as well. They feed on the organic waste products produced by the lithoautotrophs, as well as dead cells.

Microorganisms living under these conditions have developed an extraordinary ability to limit their metabolism to a level that is best measured in geologic time. Most have the ability to remain viable at miniscule to neglible metabolic cost [1]. It is because of this that the lines between life and death begin to blur. Some microbes remain metabolically dormant for such extended periods of time, that is impossible to tell whether a cell is dead or just dormant. Many individuals tend to lose the ability to reproduce after significant periods of dormancy as well [1]. It is because of these two facts that the classification of "living" or "dead" becomes a relative term when referring to deep subsurface microbes.

Dessication Resistance

As the microbes in this ecosystem use up their water reserves and have no way of replenishing, they will shrink their body size to under 1/1000 of the original volume. These dwarfed microbes are effectively termed "ultramicro-bacteria". Periods of dormancy may persist seemingly indefinitely in these stages [1].

Radiation Resistance

DNA Repair Mechanisms

Microbial processes

Subsection 1

Subsection 1a

Subsection 1b

Subsection 2

Current Research

References

[Sample reference] Takai, K., Sugai, A., Itoh, T., and Horikoshi, K. "Palaeococcus ferrophilus gen. nov., sp. nov., a barophilic, hyperthermophilic archaeon from a deep-sea hydrothermal vent chimney". International Journal of Systematic and Evolutionary Microbiology. 2000. Volume 50. p. 489-500.

[1]http://wvlc.uwaterloo.ca/biology447/modules/module6/Scientific_American_Article_Microbes.htm Fredrickson, J., Onstott, T. "Microbes Deep Inside the Earth." "Scientific American". 1996.

[2]Amend, J. P., & Teske, A. (2005). Expanding frontiers in deep subsurface microbiology. Palaeogeography, Palaeoclimatology, Palaeoecology, 219(1-2), 131-155. Elsevier. Retrieved from http://linkinghub.elsevier.com/retrieve/pii/S0031018204005954

[3] http://www.episodes.co.in/www/backissues/303/202.pdf Dong, H., Yu, B., "Geomicrobiological processes in extreme environments: A review" Episodes: Journal of International Geosciences. 2007. Volume 30. p. 202-216.

[4] http://www.microbemagazine.org/index.php/11-2009-home/1045-new-horizons-for-deep-subsurface-microbiology T. C. Onstott, F. S. Colwell, T. L. Kieft, L. Murdoch, and T. J. Phelps, "New Horizons for Deep Subsurface Microbiology". Microbe Magazine. 2009.

Edited by <Craig Mack>, a student of Angela Kent at the University of Illinois at Urbana-Champaign.